Skip to main content
Log in

The nonreciprocal heterostyly and heterotypic self-incompatibility of Ceratostigma willmottianum

  • Regular Paper – Morphology/Anatomy/Structural Biology
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Ceratostigma willmottianum (Plumbaginaceae) is a perennial herb native to China. Many species of Plumbaginaceae have been reported to exhibit heterostyly. Determining the functional breeding system of C. willmottianum can improve our understanding of the reproductive ecology of heterostylous plants. We investigated the floral traits and pollen and stigma characteristics in a natural population, and artificial pollination was carried out in an artificial population. It was found that C. willmottianum was distylous with short (S)- and long (L)-styled morphs, did not exhibit precise reciprocal herkogamy and was partially self-compatible but primarily outcrossing. In the artificial pollination experiments, the pollen tubes reached the base of the style under intermorph pollination, whereas they rarely penetrated the style under intramorph pollination and self-pollination. Both the L and S morphs exhibited a high seed set after intermorph pollination, whereas the seed set under intramorph pollination was lower. Therefore, C. willmottianum may spread the chance of receiving pollen between the two morphs by nonreciprocal heterostyly, which may be a unique mode of ecological adaptation in Plumbaginaceae. We believe that our discovery could provide new ideas regarding the origin and evolution of heterostyly.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

Self-pollination:

Self-pollination (L♀ × L♂ or S♀ × S♂)

Intrapollination:

Intramorph pollination (L♀ × L'♂ or S♀ × S'♂)

Interpollination:

Intermorph pollination (S♀ × L♂ or L♀ × S♂)

HetSI:

Heterotypic self-incompatibility

HomSI:

Homomorphic self-incompatibility

P/O ratio:

Pollen/ovule ratio

OCI:

Outcrossing index

ESEM:

Environmental scanning electron microscope

References

  • Arzani K, Nejatian MA, Karimzadeh G (2005) Apricot (Prunus armeniaca) pollen morphological characterisation through scanning electron microscopy, using multivariate analysis. New Zealand J Crop Hort Sci 33:381–388

    Article  Google Scholar 

  • Bahadur B (1970) Heterostyly in Hedyotis nigricans (Lam) Fosb. J Genetics 60:175

    Article  Google Scholar 

  • Barrett SC (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284

    Article  CAS  PubMed  Google Scholar 

  • Barrett SCH, Shore JS (2008) New insights on heterostyly: comparative biology, ecology and genetics. Self-incompatibility in flowering plants. Springer, Berlin, Heidelberg, pp 3–32

    Chapter  Google Scholar 

  • Bremer B, Manen JF (2000) Phylogeny and classification of the subfamily Rubioideae (Rubiaceae). Plant Syst Evol 225:43–72

    Article  CAS  Google Scholar 

  • Castro CC, Araujo AC (2004) Distyly and sequential pollinators of Psychotria nuda (Rubiaceae) in the Atlantic rain forest, Brazil. Plant Syst Evol 244:131–139

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1979) A model for the evolution of distyly. Am Nat 114:467–498

    Article  Google Scholar 

  • Chen L, Yang C, Huang H (2009) Comparison of detection methods for pollen viability of Hemarthria compressa. Exp Technol Manag 1:39–41

    Google Scholar 

  • Chen M, You Y, Zhang X (2010) Advances in the research of heterostyly. Acta Pratacult Sin 19:226–239

    Google Scholar 

  • Cruden RW (1977) Pollen–ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31(1):32–46

    Article  PubMed  Google Scholar 

  • Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press, Oxford

    Google Scholar 

  • Darwin C (1897) The different forms of flowers on plants of the same species. D. Appleton and Company, New York

    Google Scholar 

  • Dorken ME, Eckert CG (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89(3):339–350

    Article  Google Scholar 

  • Dulberger R (1975) Intermorph structural differences between stigmatic papillae and pollen grains in relation to incompatibility in Plumbaginaceae. Proc R Soc Lond B Biol Sci 188:257–274

    Article  Google Scholar 

  • Dulberger R (1992) Floral polymorphisms and their functional significance in the heterostylous syndrome. Evolution and function of heterostyly. Springer, Berlin, Heidelberg, pp 41–84

    Chapter  Google Scholar 

  • Dulberger R, Ornduff R (2000) Stigma morphology in distylous and non-heterostylous species of Villarsia (Menyanthaceae). Plant Syst Evol 225:171–184

    Article  Google Scholar 

  • Faivre AE, Mcdade LA (2001) Population-level variation in the expression of heterostyly in three species of Rubiaceae: does reciprocal placement of anthers and stigmas characterize heterostyly? Am J Bot 88:841–853

    Article  CAS  PubMed  Google Scholar 

  • Ferrero V, De Vega C, Stafford GI, Van Staden J, Johnson SD (2009) Heterostyly and pollinators in Plumbago auriculata (Plumbaginaceae). South Afr J Bot 75:778–784

    Article  Google Scholar 

  • Gandadikusumah VG, Wawangningrum H, Rahayu S (2017) Pollen viability of Aeschynanthus tricolor Hook. J Trop Life Sci 7:53–60

    Article  Google Scholar 

  • Ganders FR (1979) The biology of heterostyly. New Zealand J Bot 17:607–635

    Article  Google Scholar 

  • Harder LD, Johnson SD (2009) Darwin’s beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol 183:530–545

    Article  PubMed  Google Scholar 

  • Hu J, Gao S, Liu S, Hong M, Zhu Y, Wu Y et al (2019) An aseptic rapid propagation system for obtaining plumbagin of Ceratostigma willmottianum Stapf. Plant Cell Tissue Organ Cult 137:369–377

    Article  CAS  Google Scholar 

  • Jian MY, Yu Z, Jun X, Zhong WL, Han DS (1997) A new glucoside from Ceratostigma willmottianum. Chinese Chem Lett 8:873–874

    Google Scholar 

  • Kunin WE (1993) Sex and the single mustard: population density and pollinator behavior effects on seed-set. Ecology 74:2145–2160

    Article  Google Scholar 

  • Levin DA (1972) Competition for pollinator service: a stimulus for the evolution of autogamy. Evolution 26:668–669

    Article  PubMed  Google Scholar 

  • Li Y, He X, Liao S, Wang A, Lan Y, Huang Y, Wang Y (2008) Study on the preparation of chemical reference of Ceratostigma willmottianum Stapf. J Guiyang Med College 6:622–624

    Google Scholar 

  • Lloyd DG, Webb CJ (1992) The evolution of heterostyly. Evolution and function of heterostyly. Springer, Berlin, Heidelberg, pp 151–178

    Chapter  Google Scholar 

  • Lobato-de Magalhães T, Martínez M (2020) Insights into distyly and seed morphology of the aquatic plant Nymphoides fallax Ornduff (Menyanthaceae). Flora 262:151526

    Article  Google Scholar 

  • Lu QZ, Deng W, Tian HP, Li SK (2014) Study on the ethnic medicine Ceratostigma willmottianum Stapf for its analgesic and anti-inflammatory effects and acute toxicity test. Guizhou Sci 1(26–28):39

    Google Scholar 

  • Luo S, Zhang K, Zhong WP, Chen P, Fan XM, Yuan DY (2020) Optimization of in vitro pollen germination and pollen viability tests for Castanea mollissima and Castanea henryi. Sci Hort 271:109481

    Article  CAS  Google Scholar 

  • Mahmoudi M, Boughalleb F, Pellegrino G, Abdellaoui R, Nasri N (2020) Flower, seed, and fruit development in three Tunisian species of Polygonum: implications for their taxonomy and evolution of distyly in Polygonaceae. PLoS One 15:e0227099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin AJ, Bigwood RF (1969) Rapid fluorescent-antibody staining technique. Appl Microbiol 17:14–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raza J, Ahmad M, Zafar M, Athar M, Sultana S, Majeed S et al (2020) Comparative foliar anatomical and pollen morphological studies of Acanthaceae using light microscope and scanning electron microscope for effective microteaching in community. Microscopy Res Tech 83:1103–1117

    Article  CAS  Google Scholar 

  • Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467–489

    Article  CAS  PubMed  Google Scholar 

  • Tekleva M (2016) Pollen morphology and ultrastructure of several Gnetum species: an electron microscopic study. Plant Syst Evol 302:291–303

    Article  Google Scholar 

  • Washitani I, Osawa R, Namai H, Niwa M (1994) Patterns of female fertility in heterostylous Primula sieboldii under severe pollinator limitation. J Ecol 82:571–579

    Article  Google Scholar 

  • Watanabe K, Yang TA, Nishihara C, Huang TL, Nakamura K, Peng CI, Sugawara T (2015) Distyly and floral morphology of Psychotria cephalophora (Rubiaceae) on the oceanic Lanyu (Orchid) Island. Taiwan Bot Stud 56:10

    Article  PubMed  Google Scholar 

  • Weller SG, Ornduff R (1977) Cryptic self-incompatibility in Amsinckia grandiflora. Evolution 31(1):47–51

    PubMed  Google Scholar 

  • Xu XY, Zhou LL, Wang ZK, Zhuang L (2015) Flower distyly and breeding system of Limonium chrysocomum. Bulletin Bot Res 35(6):883–890

    Google Scholar 

  • Yang CD, He XZ, Gou GQ (2018) Ophiorrhiza guizhouensis (Rubiaceae), a new species from Guizhou Province, southwestern China. PhytoKeys 95:121

    Article  Google Scholar 

  • Zhang S, Gao SP (2014) Distyly and selfing incompatibility of Plumbago auriculata. Guihaia 34:747–753

    CAS  Google Scholar 

  • Zhang W, Zhou B, Xiao Y, Yan X, Zhang Z, Li X (2013) Reproductive ecology of distylous Fagopyrum dibotrys. Acta Bot Boreali-Occidental Sin 33:483–493

    CAS  Google Scholar 

  • Zhang C, Wang LL, Duan YW, Lan D, Yang YP (2014) Pollination ecology of Arnebia szechenyi (Boraginaceae), a Chinese endemic perennial characterized by distyly and heteromorphic self-incompatibility. Ann Bot Fennici 51:297–304

    Article  Google Scholar 

Download references

Funding

National Key R&D Program of China (2018YFD0600105). Sichuan Science and Technology Program (2016NYZ0038).

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization, Suping Gao; methodology, Meiting Hong; validation, Ting Lei; formal analysis, Wenji Li.; investigation, Ping Shen; data curation, Jiani Li; writing—original draft preparation, Wenji Li and Meiting Hong; writing—review and editing, Suping Gao; supervision, Mingyan Jiang; project administration, Yifan Duan and Lisha Shi.

Corresponding author

Correspondence to Suping Gao.

Ethics declarations

Conflicts of interest

The authors have no conflicts of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, S., Li, W., Hong, M. et al. The nonreciprocal heterostyly and heterotypic self-incompatibility of Ceratostigma willmottianum. J Plant Res 134, 543–557 (2021). https://doi.org/10.1007/s10265-021-01269-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-021-01269-5

Keywords

Navigation